Platelet-rich plasma to treat experimentally-induced skin wounds in animals: A systematic review and meta-analysis

Adolfo Maria Tambella, Anna Rita Attili, Gilles Dupré, Andrea Cantalamessa, Stefano Martin, Vincenzo Cuteri, Sabrina Marcazzan, Massimo Del Fabbro, Adolfo Maria Tambella, Anna Rita Attili, Gilles Dupré, Andrea Cantalamessa, Stefano Martin, Vincenzo Cuteri, Sabrina Marcazzan, Massimo Del Fabbro

Abstract

The objective of the study was to review current literature to determine whether the topical application of platelet-rich plasma (PRP) promotes healing in experimentally-induced full-thickness skin wounds in animals. The hypothesis was that the adjunct of PRP has a positive effect on wound healing. An electronic search was carried out on the following databases: Web of Science, Cochrane Library, PubMed, Research Gate, Cochrane Wounds Group, Veterinary Information Network. No publication date nor language restrictions were applied. Randomised and not randomised controlled clinical trials comparing PRP with placebo or with other treatments were included. The reduction of open wound area in PRP-treated (test) wounds compared to control wounds was the primary outcome. Secondary outcomes were healing time and number of healed cases in test group compared to control. The following effect sizes were calculated: the Hedges' g for continuous variables; the odds ratio for binary data. Eighteen controlled clinical trials were included in the qualitative and quantitative synthesis, with a total of 661 wounds. All studies were published in the period 2007-2016. Eight studies were carried out on rodent/lagomorph mammals and 10 on non-rodent/lagomorph mammals. In all included studies, control wounds underwent placebo or were left untreated. The PRP group showed a better healing performance than the control group in each outcome. The effect size was statistically significant considering the primary outcome and the overall aggregation of the three outcomes. The effect size, although in favour of the treatment with PRP, was not significant considering the healing time and the number of healings. The overall heterogeneity was mild or moderate. Five studies reported a high risk of selection bias. The publication bias was always mild or absent. The results support the hypothesis of the positive effects of the PRP when compared to control groups in the treatment of experimentally-induced full-thickness skin wounds in animals. PRP can therefore be considered an effective adjunctive therapy in stimulating second intention healing of acute wounds in healthy animals.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Selection of primary studies: PRISMA…
Fig 1. Selection of primary studies: PRISMA flow diagram.
Fig 2. Risk of bias summary.
Fig 2. Risk of bias summary.
Review author’s judgement obtained by each included study for each type of bias.
Fig 3. Forest plot: PRP vs control,…
Fig 3. Forest plot: PRP vs control, meta-analysis 1: Reduction of open wound area (negative ES, positioned on the left of the null value: favours control; positive ES, positioned on the right of the null value: favours PRP).
Heterogeneity analysis: Q = 39.35; df = 14; P = 0.000; I2 = 64.42; T2 = 0.14; T = 0.37. (ES: effect size; 95%CI: confidence interval; W: weight; V: variance; SE: standard error; Sig: statistical significance (p-value); N: total sample size; N1: sample size PRP group; N2: sample size control group; Q, I2, T2 and T: indexes of heterogeneity; df: degrees of freedom).
Fig 4. Sensitivity analysis, meta-analysis 1: Reduction…
Fig 4. Sensitivity analysis, meta-analysis 1: Reduction of open wound area.
(ES: effect size; 95%CI: confidence interval; W: weight; V: variance; SE: standard error; Sig: statistical significance (p-value); N: total sample size; N1: sample size PRP group; N2: sample size control group).
Fig 5. Publication bias analysis, funnel plot,…
Fig 5. Publication bias analysis, funnel plot, meta-analysis 1: Reduction of open wound area.
Trim and fill analysis: trimmed studies = 0. Overall effect size (observed): ES = 0.40; LL = 0.16; UL = 0.65; P = 0.001; V = 0.02; SE = 0.13. Overall effect size (estimated): ES = 0.40; LL = 0.16; UL = 0.65; P = 0.001; V = 0.02; SE = 0.13. Egger’s linear regression test: intercept = 0.60; t = 0.52; P = 0.611.
Fig 6. Forest plot: PRP vs control,…
Fig 6. Forest plot: PRP vs control, meta-analysis 2: Healing time (negative ES, positioned on the left of the null value: favours control; positive ES, positioned on the right of the null value: favours PRP).
Heterogeneity analysis: Q = 13.69; df = 3; P = 0.003; I2 = 78.09; T2 = 0.50; T = 0.71. (ES: effect size; 95%CI: confidence interval; W: weight; V: variance; SE: standard error; Sig: statistical significance (p-value); N: total sample size; Q, I2, T2 and T: indexes of heterogeneity; df: degrees of freedom).
Fig 7. Sensitivity analysis, meta-analysis 2: Healing…
Fig 7. Sensitivity analysis, meta-analysis 2: Healing time.
(ES: effect size; 95%CI: confidence interval; W: weight; V: variance; SE: standard error; Sig: statistical significance (p-value); N: total sample size; N1: sample size PRP group; N2: sample size control group).
Fig 8. Publication bias analysis, funnel plot,…
Fig 8. Publication bias analysis, funnel plot, meta-analysis 2: Healing time.
Trim and fill analysis: trimmed studies = 0. Overall effect size (observed): ES = 0.10; LL = -0.68; UL = 0.89; P = 0.795; V = 0.16; SE = 0.40. Overall effect size (estimated): ES = 0.10; LL = -0.68; UL = 0.89; P = 0.795; V = 0.16; SE = 0.40. Egger’s linear regression test: intercept = -21.36; t = -2.66; P = 0.117.
Fig 9. Forest plot: PRP vs control,…
Fig 9. Forest plot: PRP vs control, meta-analysis 3: Number of healings (negative ES, positioned on the left of the null value: favours control; positive ES, positioned on the right of the null value: favours PRP).
Heterogeneity analysis: Q = 7.59; df = 1; P = 0.006; I2 = 86.82; T2 = 1.68; T = 1.30. (ES: effect size; 95%CI: confidence interval; W: weight; V: variance; SE: standard error; Sig: statistical significance (p-value); N: total sample size; N1: sample size PRP group; N2: sample size control group; Q, I2, T2 and T: indexes of heterogeneity; df: degrees of freedom).
Fig 10. Forest plot: PRP vs control,…
Fig 10. Forest plot: PRP vs control, meta-analysis 4: Combination of all outcomes (negative ES, positioned on the left of the null value: favours control; positive ES, positioned on the right of the null value: favours PRP).
Heterogeneity analysis: Q = 50.87; df = 17; P = 0.000; I2 = 66.58; T2 = 0.16; T = 0.40. (ES: effect size; 95%CI: confidence interval; W: weight; V: variance; SE: standard error; Sig: statistical significance (p-value); N: total sample size; Q, I2, T2 and T: indexes of heterogeneity; df: degrees of freedom).
Fig 11. Sensitivity analysis, meta-analysis 4: Combination…
Fig 11. Sensitivity analysis, meta-analysis 4: Combination of all outcomes.
(ES: effect size; 95%CI: confidence interval; W: weight; V: variance; SE: standard error; Sig: statistical significance (p-value); N: total sample size; N1: sample size PRP group; N2: sample size control group).
Fig 12. Publication bias analysis, funnel plot,…
Fig 12. Publication bias analysis, funnel plot, meta-analysis 4: Combination of all outcomes.
Trim and fill analysis: trimmed studies = 0. Overall effect size (observed): ES = 0.40; LL = 0.16; UL = 0.64; P = 0.001; V = 0.01; SE = 0.12. Overall effect size (estimated): ES = 0.40; LL = 0.16; UL = 0.64; P = 0.001; V = 0.01; SE = 0.12. Egger’s linear regression test: intercept = 0.63; t = 0.57; P = 0.577.

References

    1. Knighton DR, Ciresi KF, Fiegel VD, Austin LL, Butler EL. Classification and treatment of chronic nonhealing wounds. Successful treatment with autologous platelet—derived wound healing factors (PDWHF). Ann Surg. 1986; 204(3):322–330.
    1. Mast BA, Schultz GS. Interaction of cytokines, growth factors, and protease in acute and chronic wounds. Wound Repair Regen. 1996; 4:411–420. 10.1046/j.1524-475X.1996.40404.x
    1. Tarnuzzer RW, Schultz GS. Biochemical analysis of acute and chronic wound environments. Wound Repair Regen. 1996; 4:321–325. 10.1046/j.1524-475X.1996.40307.x
    1. Stadelmann WK, Digenis AG, Tobin GR. Physiology and healing dynamics of chronic cutaneous wounds. Am J Surg (Suppl 2A). 1998; 176:26S–38S.
    1. Rožman P, Bolta Z. Use of platelet growth factors in treating wounds and soft-tissue injuries. Acta Dermatovenerol Alp Pannonica Adriat. 2007; 16(4):156–165.
    1. Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev. 2003; 83:835–870. 10.1152/physrev.2003.83.3.835
    1. Robson MC. The role of growth factors in the healing of chronic wounds. Wound Repair Regen. 1997; 5(1):12–17. 10.1046/j.1524-475X.1997.50106.x
    1. Crovetti G, Martinelli G, Issi M, Barone M, Guizzardi M, Campanati B, et al. Platelet gel for healing cutaneous chronic wounds. Transfus Apher Sci. 2004; 30:145–151. 10.1016/j.transci.2004.01.004
    1. Mazzucco L, Borzini P, Gope R. Platelet-derived factors involved in tissue repair—from signal to function. Transfus Med Rev. 2010; 24(3):218–234. 10.1016/j.tmrv.2010.03.004
    1. Anitua E, Alkhraisat MH, Orive G. Perspectives and challenges in regenerative medicine using plasma rich in growth factors. J Control Release. 2012; 157:29–38. 10.1016/j.jconrel.2011.07.004
    1. Landesberg R, Martin Roy M, Glickmann RS. Quantification of growth factor levels using a simplified method of platelet-rich plasma gel preparation. J Oral Maxillofac Surg. 2000; 58:297–300. 10.1016/S0278-2391(00)90058-2.
    1. Carter CA, Jolly DG, Worden CE Sr, Hendren DG, Kaneb CJM. Platelet-rich plasma gel promotes differentiation and regeneration during equine wound healing. Exp Mol Pathol. 2003; 74:244–255. 10.1016/S0014-4800(03)00017-0.
    1. Martineau I, La Coste E, Gagnon G. Effects of calcium and thrombin on growth factor release from platelet concentrates: kinetics and regulation of endothelial cell proliferation. Biomaterials. 2004; 25:4489–4502. 10.1016/j.biomaterials.2003.11.013
    1. Leitner GC, Gruber R, Neumüller J, Wagner A, Kloimstein P, Höcker P, et al. Platelet content and growth factor release in platelet‐rich plasma: a comparison of four different systems. Vox Sang. 2006; 91:135–139. 10.1111/j.1423-0410.2006.00815.x
    1. Rughetti A, Gallo R, Caloprisco G, Borean A, Necozione S, Dell’Orso L, et al. Platelet gel: assays of three growth factors. Blood Transfus. 2006; 4:92–101.
    1. Semple E, Speck ER, Aslam R, Kim M, Kumar V, Semple JW. Evaluation of platelet gel characteristics using thrombin produced by the thrombin processing device: a comparative study. J Oral Maxillofac Surg. 2008; 66:632–638. 10.1016/j.joms.2007.06.623
    1. Dohan Ehrenfest DM, Rasmusson L, Albrektsson T. Classification of platelet concentrates: from pure platelet-rich plasma (P-PRP) to leucocyte- and platelet-rich fibrin (L-PRF). Trends Biotechnol. 2009; 27(3):158–167. 10.1016/j.tibtech.2008.11.009
    1. Anitua E, Zalduendo MM, Alkhraisat MH, Orive G. Release kinetics of platelet-derived and plasma-derived growth factors from autologous plasma rich in growth factors. Ann Anat. 2013; 195:461–466. 10.1016/j.aanat.2013.04.004
    1. Giraldo CE, López C, Álvarez ME, Samudio IJ, Prades M, Carmona JU. Effects of the breed, sex and age on cellular content and growth factor release from equine pure-platelet rich plasma and pure platelet rich gel. BMC Vet Res. 2013; 9:29 10.1186/1746-6148-9-29
    1. Steed DL, Goslen JB, Holloway GA, Malone JM, Bunt TJ, Webster MW. Randomized prospective double‐blind trial in healing chronic diabetic foot ulcers. CT‐102 activated platelet supernatant, topical versus placebo. Diabetes Care. 1992; 15:1598–1604. 10.2337/diacare.15.11.1598.
    1. Mazzucco L, Medici D, Serra M, Panizza R, Rivara G, Orecchia S, et al. The use of autologous platelet gel to treat difficult—to—heal wounds: a pilot study. Transfusion. 2004; 44:1013–1018. 10.1111/j.1537-2995.2004.03366.x
    1. Borzini P, Mazzucco L. Tissue regeneration and in loco administration of platelet derivatives: clinical outcome, heterogeneous products, and heterogeneity of the effector mechanisms. Transfusion. 2005; 45:1759–1767. 10.1111/j.1537-2995.2005.00600.x
    1. O’Connel SM, Impeduglia T, Hessler K, Wang XJ, Carroll RJ, Dardik H. Autologous platelet‐rich fibrin matrix as cell therapy in the healing of chronic lower‐extremity ulcers. Wound Repair Regen. 2008; 16:749–756. 10.1111/j.1524-475X.2008.00426.x
    1. Marx RE, Carlson ER, Eichstaedt RM, Schimmele SR, Strauss JE, Georgeff KR. Platelet‐rich plasma: growth factor enhancement for bone grafts. Oral Surg, Oral Med, Oral Pathol, Oral Radiol Endod. 1998; 85:638–646. 10.1016/S1079-2104(98)90029-4.
    1. Mei-Dan O, Carmont MR. Novel applications of platelet-rich plasma technology in musculoskeletal medicine and surgery. Oper Tech Orthop. 2012; 22:56–63. 10.1053/j.oto.2011.10.005.
    1. DeRossi R, Coelho ACAO, Mello GS, Frazílio FO, Leal CRB, Facco GG, et al. Effects of platelet-rich plasma gel on skin healing in surgical wound in horses. Acta Cir Bras. 2009; 24(4):276–281. 10.1590/S0102-86502009000400006.
    1. Kim JH, Park C, Park HM. Curative effect of autologous platelet-rich plasma on a large cutaneous lesion in a dog. Vet Dermatol. 2009; 20(2):123–126. 10.1111/j.1365-3164.2008.00711.x
    1. Rabillard M, Grand JG, Dalibert E, Fellah B, Gauthier O, Niebauer GW. Effects of autologous platelet rich plasma gel and calcium phosphate biomaterials on bone healing in a ulnar ostectomy model in dogs. Vet Comp Orthop Traumatol. 2009; 22:460–466. 10.3415/VCOT-09-04-0048
    1. Fresno L, Fondevila D, Bambo O, Chacaltana A, García F, Andaluz A. Effect of platelet‐rich plasma on intestinal wound healing in pigs. Vet J. 2010; 185:322–327. 10.1016/j.tvjl.2009.06.009
    1. Sardari K, Emami MR, Kazemi H, Movasagi AR, Goli AA, Lotfi A, et al. Effects of platelet-rich plasma (PRP) on cutaneous regeneration and wound healing in dogs treated with dexamethasone. Comp Clin Pathol 2011; 20:155–162. 10.1007/s00580-010-0972-y
    1. Visser LC, Arnoczky SP, Caballero O, Gardner KL. Evaluation of the use of an autologous platelet‐rich fibrin membrane to enhance tendon healing in dogs. Am J Vet Res. 2011; 72:699–705. 10.2460/ajvr.72.5.699
    1. Iacopetti I, Perazzi A, Ferrari V, Busetto R. Application of platelet-rich gel to enhance wound healing in the horse: a case report. J Equine Vet Sci. 2012; 32:123–128. 10.1016/j.jevs.2011.08.012.
    1. Maciel FB, DeRossi R, Módolo TJC, Pagliosa RC, Leal CRJ, Delben AAAST. Scanning electron microscopy and microbiological evaluation of equine burn wound repair after platelet-rich plasma gel treatment. Burns. 2012; 38:1058–1065. 10.1016/j.burns.2012.02.029
    1. Suaid FF, Carvalho MD, Ambrosano GMB, Nociti FH Jr, Casati MZ, Sallum SA. Platelet-rich plasma in the treatment of class II furcation defects: a histometrical study in dogs. J Applied Oral Sci. 2012; 20:162–169. 10.1590/S1678-77572012000200007.
    1. Tambella AM, Attili AR, Dini F, Palumbo Piccionello A, Vullo C, Serri E, et al. Autologous platelet gel to treat chronic decubital ulcers: a randomized, blind controlled clinical trial in dogs. Vet Surg. 2014; 43:726–733. 10.1111/j.1532-950X.2014.12148.x
    1. Moher D, Liberati A, Tetzlaff J, Altman DG; The PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 2009; 6:e1000097 10.1371/journal.pmed.1000097
    1. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med. 2009; 6(7):e1000100 10.1371/journal.pmed.1000100
    1. Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews of Interventions. Version 5.1.0. The Cochrane Collaboration; 2011. .
    1. Crocetti E. Rassegne sistematiche, sintesi della ricerca e meta-analisi. North Charleston, SC, USA: CreateSpace; 2015.
    1. Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002; 21:1539–1558. 10.1002/sim.1186
    1. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. Br Med J. 2003; 327(7414):557–560. 10.1136/bmj.327.7414.557
    1. Abegão KGB, Bracale BN, Delfim IG, dos Santos ES, Laposy CB, Nai GA, et al. Effects of heterologous platelet-rich plasma gel on standardized dermal wound healing in rabbits. Acta Cir Bras. 2015; 30(3):209–215. 10.1590/S0102-865020150030000008
    1. Al-Bayati AH, Al-Asadi RN, Mahdi AK, Al-Falahi NH. Effects of Autologous Platelets Rich Plasma on Full-thickness Cutaneous Wounds Healing in Goats. Int J Anim Vet Adv. 2013; 5(6):233–239.
    1. Barrionuevo DV, Laposy CB, Abegão KGB, Nogueira RMB, Nai GA, Bracale BN, et al.: Comparison of experimentally-induced wounds in rabbits treated with different sources of platelet-rich plasma. Lab Anim. 2015; 49(3):209–214. 10.1177/0023677214567747
    1. Bauer JA, Correa L, Lima FLM, Lima LAPA, Pustiglioni FE. Efeitos do plasma rico em plaquetas no processo de reparação de feridas dérmicas padronizadas em ratos. R Periodontia. 2009; 19(3):98–108.
    1. Blanton MW, Hadad I, Johnstone BH, Mund JA, Rogers PI, Eppley BL, et al. Adipose Stromal Cells and Platelet-Rich Plasma Therapies Synergistically Increase Revascularization during Wound Healing. Plast Reconstr Surg. 2009; 123(Suppl.2S):56S–64S. 10.1097/PRS.0b013e318191be2d
    1. De Souza MV, Silva MB, de Oliveira Pinto J, de Souza Lima MB, Crepaldi J, Lopes GFM, et al. Immunohistochemical Expression of Collagens in the Skin of Horses Treated with Leukocyte-Poor Platelet-Rich Plasma. BioMed Res Int. 2015; Article ID 893485:1–12. 10.1155/2015/893485.
    1. Dionyssiou D, Demiri E, Foroglou P, Cheva A, Saratzis N, Aivazidis C, et al. The effectiveness of intralesional injection of platelet-rich plasma in accelerating the healing of chronic ulcers: an experimental and clinical study. Int Wound J. 2013; 10:397–406. 10.1111/j.1742-481X.2012.00996.x
    1. Hadad I, Johnstone BH, Brabham JG, Blanton MW, Rogers PI, Fellers C, et al. Development of a porcine delayed wound-healing model and its use in testing a novel cell-based therapy. Int J Radiat Oncol Biol Phys. 2010; 78(3):888–896. 10.1016/j.ijrobp.2010.05.002
    1. Jee CH, Eom NY, Jang HM, Choi ES, Won JH, Hong IH, et al. Effect of autologous platelet-rich plasma application on cutaneous wound healing in dogs. J Vet Sci. 2016; 17(1):78–87. 10.4142/jvs.2016.17.1.79.
    1. Karayannopoulou M, Psalla D, Kazakos G, Loukopoulos P, Giannakas N, Savvas I, et al. Effect of locally injected autologous platelet-rich plasma on second intention wound healing of acute full-thickness skin defects in dogs. Vet Comp Orthop Traumatol. 2015; 28:172–178. 10.3415/VCOT-14-06-0088.
    1. Lee HW, Reddy MS, Geurs N, Palcanis KG, Lemons JE, Rahemtulla FG, et al. Efficacy of platelet-rich plasma on wound healing in rabbits. J Periodontol. 2008; 79:691–696. 10.1902/jop.2008.070449
    1. Monteiro SO, Lepage OM, Theoret CL. Effects of platelet-rich plasma on the repair of wounds on the distal aspect of the forelimb in horses. Am J Vet Res. 2009; 70:277–282. 10.2460/ajvr.70.2.277
    1. Nisbet OH, Nisbet C, Yarim M, Ozak A. The Efficacy of Platelet-rich Plasma Gel and Topical Estradiol Alone or in Combination on Healing of Full-thickness Wounds. Wounds. 2009; 21(7):183–191.
    1. Notodihardjo PV, Morimoto N, Kakudo N, Matsui M, Sakamoto M, Liem PH, et al. Gelatin hydrogel impregnated with platelet-rich plasma releasate promotes angiogenesis and wound healing in murine model. J Artif Organs. 2015; 18(1):64–71. 10.1007/s10047-014-0795-8
    1. Vermeulen P, Dickens S, Degezelle K, Van den Berge S, Hendrickx B, Vranckx JJ. A plasma-based biomatrix mixed with endothelial progenitor cells and keratinocytes promotes matrix formation, angiogenesis, and reepithelialization in full-thickness wounds. Tissue Eng. 2009; 15(7):1533–1542.
    1. Yan Y, Larson DL. Acceleration of full-thickness wound healing in porcine model by autologous platelet gel. Wounds. 2007; 19(4):79–86.
    1. Yang HS, Shin J, Bhang SH, Shin JY, Park J, Im GI, et al. Enhanced skin wound healing by a sustained release of growth factors contained in platelet-rich plasma. Exp Mol Med. 2011; 43(11):622–629. 10.3858/emm.2011.43.11.070
    1. Chung T, Baek D, Kim N, Park J, Park C. Topical allogeneic platelet-rich plasma treatment for a massive cutaneous lesion induced by disseminated intravascular coagulation in a toy breed dog. Ir Vet J. 2015; 68:1–4.
    1. Demidova-Rice TN, Wolf L, Deckenback J, Hamblin MR, Herman IM. Human platelet-rich plasma- and extracellular matrix-derived peptides promote impaired cutaneous wound healing in vivo. PLoS One. 2012; 7(2):e32146 10.1371/journal.pone.0032146
    1. Ferdousy RN, Rahman MM, Paul S, Khan AHNA. Role of platelet rich plasma gel in the wound healing of black Bengal goat. IOSR Journal of Agriculture and Veterinary Science. 2013; 6(5):14–21.
    1. Henderson JL, Cupp CL, Ross EV, Shick PC, Keefe MA, Wester DC, et al. The effects of autologous platelet gel on wound healing. Ear Nose Throat J. 2003; 82(8):598–602.
    1. Hermeto LC, DeRossi R, de Pádua SB, Pontes ERJ, Santana AE. Comparative study between fibrin glue and platelet rich plasma in dogs skin grafts. Acta Cir Bras. 2012; 27(11):789–794.
    1. Koempel JA, Gibson SE, O’Grady K, Toriumi DM. The effect of platelet-derived growth factor on tracheal wound healing. Int J Pediatr Otorhinolaryngol. 1998; 46;1–8.
    1. Lian Z, Yin X, Li H, Jia L, He Xiuzhen, Yan Yongbo, et al. Synergistic effect of bone marrow-derived mesenchymal stem cells and platelet-rich plasma in streptozotocin-induced diabetic rats. Ann Dermatol. 2014; 26(1):1–10. 10.5021/ad.2014.26.1.1
    1. López C, Carmona JU. Platelet-rich plasma as an adjunctive therapy for the management of a severe chronic distal limb wound in a foal. J Equine Vet Sci. 2014; 34:1128–1133. 10.1016/j.jevs.2014.06.007.
    1. Molina-Miñano F, López-Jornet Péa, Camacho-Alonso F, Vicente-Ortega V. The use of plasma rich in growth factors on wound healing in the skin: experimental study in rabbits. Int Wound J. 2009; 6:145–148. 10.1111/j.1742-481X.2009.00592.x
    1. Ostvar O, Shadvar S, Yahaghi E, Azma K, Fayyaz AF, Ahmadi K, et al. Effect of platelet-rich plasma on the healing of cutaneous defects exposed to acute to chronic wounds: a clinico-histopathologic study in rabbits. Diagn Pathol. 2015; 10(85):1–6. 10.1186/s13000-015-0327-8
    1. Pietramaggiori G, Kaipainen A, Czeczuga JH, Wagner CT, Orgill DP. Freeze-dried platelet-rich plasma shows beneficial healing properties in chronic wounds. Wound Rep Reg. 2006; 14:573–580. 10.1111/j.1743-6109.2006.00164.x
    1. Pietramaggiori G, Scherer SS, Mathews JC, Alperovich M, Yang HJ, Neuwalder J, et al. Healing modulation induced by freeze-dried platelet-rich plasma and micronized allogenic dermis in a diabetic wound model. Wound Rep Reg. 2008; 16:218–225. 10.1111/j.1524-475X.2008.00362.x
    1. Sell SA, Wolfe PS, Spence AJ, Rodriguez IA, McCool JM, Petrella RL, et al. A preliminary study on the potential of manuka honey and platelet-rich plasma in wound healing. Int J Biomater. 2012; 313781:1–14. 10.1155/2012/313781
    1. Shayesteh YS, Eshghyar N, Moslemi N, Dehghan MM, Motahhary P, Ghobadi Z, et al. The effect of platelet-rich plasma on healing of palatal donor site following connective tissue harvesting: a pilot study in dogs. Clin Implant Dent Relat Res. 2012; 14(3):428–433. 10.1111/j.1708-8208.2009.00263.x
    1. Tsuzuki N, Seo JP, Yamada K, Haneda S, Tabata Y, Sasaki Naoki. Effect of compound of gelatin hydrogel microsphere incorporated with platelet-rich plasma and alginate on sole defect in cattle. J Vet Med Sci. 2012; 74(8):1041–1044. 10.1292/jvms.11-0495
    1. Vijayaraghavan N, Mohapatra DP, Friji MT, Kumar D, Arjun A, Bibilash BS, et al. Role of autologous platelet rich plasma (APRP) in wound healing. Journal of the Society for Wound Care and Research. 2014; 7(1):23–28.
    1. Zubin E, Conti V, Leonardi F, Zanichelli S, Ramoni R, Grolli S. Regenerative therapy for the management of a large skin wound in a dog. Clin Case Rep. 2015; 3(7):598–603. 10.1002/ccr3.253
    1. Cochrane CA, Freeman KL, Knottenbelt DC. Effect of growth factors on the characteristics of cells associated with equine wound healing and sarcoid formation. Wound Repair Regen. 1996; 4(1): 58–65. 10.1046/j.1524-475X.1996.40111.x
    1. Sørensen MA, Petersen LJ, Bundgaard L, Toft N, Jacobsen S. Regional disturbances in blood flow and metabolism in equine limb wound healing with formation of exuberant granulation tissue. Wound Repair Regen. 2014; 22(5): 647–653. 10.1111/wrr.12207
    1. Als-Nielsen B, Chen W, Gluud C, Kjaergard LL. Association of funding and conclusions in randomized drug trials: a reflection of treatment effect or adverse event?. JAMA. 2003; 290(7): 921–928. 10.1001/jama.290.7.921
    1. Lesser LI, Ebbeling CB, Goozner M, Ludwig DS. Relationship between funding source and conclusion among nutrition-related scientific articles. PLoS Med. 2007; 4(1):e5 10.1371/journal.pmed.0040005
    1. Falk Delgado A, Falk Delgado A. The association of funding source on effect size in randomized controlled trials: 2013–2015 –a cross-sectional survey and meta-analysis. Trials. 2017; 18(1): 125 10.1186/s13063-017-1872-0
    1. Mazzucco L, Balbo V, Guaschino R. ‘‘Reasonable compromise” to define the quality standards of platelet concentrate for non-transfusion use (CPunT). Transfus Apher Sci. 2012; 47:207–211. 10.1016/j.transci.2012.06.006
    1. Weibrich G, Kleis WKG, Hafner G, Hitzler WE. Growth factor levels in platelet-rich plasma and correlations with donor age, sex, and platelet count. J Craniomaxillofac Surg. 2002; 30:97–102. 10.1054/jcms.2002.0285
    1. McCarrel T, Lisa Fortier L. Temporal growth factor release from platelet-rich plasma, trehalose lyophilized platelets, and bone marrow aspirate and their effect on tendon and ligament gene expression. J Orthop Res. 2009; 27(8):1033–1042. 10.1002/jor.20853
    1. Giusti I, Rughetti A, D’Ascenzo S, Millimaggi D, Pavan A, Dell’Orso L, et al. Identification of an optimal concentration of platelet gel for promoting angiogenesis in human endothelial cells. Transfusion. 2009; 49:771–778. 10.1111/j.1537-2995.2008.02033.x
    1. Brossi PM, Moreira JJ, Machado TSL, Baccarin RYA. Platelet-rich plasma in orthopedic therapy: a comparative systematic review of clinical and experimental data in equine and human musculoskeletal lesions. BMC Vet Res. 2015; 11(98):1–17. 10.1186/s12917-015-0403-z
    1. Chang KV, Hung CY, Aliwarga F, Wang TG, Han DS, Chen WS. Comparative effectiveness of platelet-rich plasma injections for treating knee joint cartilage degenerative pathology: a systematic review and meta-analysis. Arch Phys Med Rehabil. 2014; 95:562–575. 10.1016/j.apmr.2013.11.006
    1. Del Fabbro M, Corbella S, Taschieri S, Francetti L, Weinstein R. Autologous platelet concentrate for post-extraction socket healing: a systematic review. Eur J Oral Implantol. 2014; 7:333–344.
    1. Del Fabbro M, Gallesio G, Mozzati M. Autologous platelet concentrates for bisphosphonate-related osteonecrosis of the jaw treatment and prevention: a systematic review of the literature. Eur J Canc. 2015; 51:62–74. 10.1016/j.ejca.2014.10.015.
    1. Laudy ABM, Bakker EWP, Rekers M, Moen MH: Efficacy of platelet-rich plasma injections in osteoarthritis of the knee: a systematic review and meta-analysis. Br J Sports Med. 2015; 49:657–672. 10.1136/bjsports-2014-094036
    1. Martinez-Zapata MJ, Martí-Carvajal AJ, Solà I, Expósito JA, Bolíbar I, Rodríguez L, et al. Autologous platelet-rich plasma for treating chronic wounds. Cochrane Database Syst Rev. 2016; 5(CD006899):1–66. 10.1002/14651858.CD006899.pub3

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